Advertisement

Behavioral responses to ocean acidification in marine invertebrates: new insights and future directions

  • Ting Wang
  • Youji WangEmail author
Article

Abstract

Ocean acidification (OA) affects marine biodiversity and alters the structure and function of marine populations, communities, and ecosystems. Recently, effects of OA on the behavioral responses of marine animals have been given with much attention. While many of previous studies focuses on marine fish. Evidence suggests that marine invertebrate behaviors were also be affected. In this review, we discussed the effects of C02-driven OA on the most common behaviors studied in marine invertebrates, including settlement and habitat selection, feeding, anti-predatory, and swimming behaviors, and explored the related mechanisms behind behaviors. This review summarizes how OA affects marine invertebrate behavior, and provides new insights and highlights novel areas for future research.

Keywords

carbon dioxide global climate change invertebrate behavior ocean acidification (OA) pH 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgement

We are grateful to Dr. Jeff Clements, Dr. Sam Dupont, and two anonymous reviewers for their valuable comments and revisions for this review.

References

  1. Albright R, Langdon C. 2011. Ocean acidification impacts multiple early life history processes of the Caribbean coral Porites astreoides. Global Change Biol., 17(7): 2478–2487,  https://doi.org/10.1111/j.1365-2486.2011.02404.x.CrossRefGoogle Scholar
  2. Albright R, Mason B, Langdon C J. 2008. Effect of aragonite saturation state on settlement and post-settlement growth of Porites astreoides larvae. Coral Reefs, 27(3): 485–490,  https://doi.org/10.1007/s00338-008-0392-5.CrossRefGoogle Scholar
  3. Albright R, Mason B, Miller M, Langdon C. 2010. Ocean acidification compromises recruitment success of the threatened Caribbean coral Acroporapalmata. Proc. Natl. Acad. Sci. USA, 107(47): 20400–20404,  https://doi.org/10.1073/pnas.l007273107.CrossRefGoogle Scholar
  4. Alenius B, Munguia P. 2012. Effects of pH variability on the intertidal isopod, Paradella dianae. Mar. Freshw. Behav. Physiol, 45(4): 245–259,  https://doi.org/10.1080/10236244.2012.727235.CrossRefGoogle Scholar
  5. Amaral V, Cabral H N, Bishop M J. 2012. Effects of estuarine acidification on predator-prey interactions. Mar. Ecol. Prog. Ser, 445: 117–127,  https://doi.org/10.3354/meps09487.CrossRefGoogle Scholar
  6. Anlauf H, D’Croz L, O’Dea A. 2011. A corrosive concoction: the combined effects of ocean warming and acidification on the early growth of a stony coral are multiplicative. J. Exp. Mar. Biol. Ecol, 397(1): 13–20,  https://doi.org/10.1016/j.jembe.2010.11.009.CrossRefGoogle Scholar
  7. Appelhans Y S, Thomsen J, Opitz S, Pansch C, Melzner F, Wahl M. 2014. Juvenile sea stars exposed to acidification decrease feeding and growth with no acclimation potential. Mar. Ecol. Prog. Ser, 509: 227–239,  https://doi.org/10.3354/mepsl0884.CrossRefGoogle Scholar
  8. Appelhans Y S, Thomsen J, Pansch C, Melzner F, Wahl M. 2012. Sourtimes: seawater acidification effects on growth, feeding behaviour and acid-base status of Asterias rubens and Carcinus maenas. Mar. Ecol. Prog. Ser., 459: 85–98,  https://doi.org/10.3354/meps09697.CrossRefGoogle Scholar
  9. Ashur M M, Johnston N K, Dixson D L. 2017. Impacts of ocean acidification on sensory function in marine organisms. Integr. Comp. Biol., 57(1): 63–80,  https://doi.org/10.1093/icb/icx010.CrossRefGoogle Scholar
  10. Barry J P, Lovera C, Buck K R, Peltzer E T, Taylor J R, Walz P, Whaling P J, Brewer P G. 2014. Use of a free ocean CO2 enrichment (FOCE) system to evaluate the effects of ocean acidification on the foraging behavior of a deep-sea urchin. Environ. Sci. Technoi, 48(16): 9890–9897,  https://doi.org/10.1021/es501603r.CrossRefGoogle Scholar
  11. Benítez S, Duarte C, Lopez J, Manríquez P H, Navarro J M, Bonta C C, Torres R, Quijón P A. 2016. Ontogenetic variability in the feeding behavior of a marine amphipod in response to ocean acidification. Mar. Pollut. Bull., 112(1-2): 375–379,  https://doi.org/10.1016/j.marpolbul.2016.07.016.CrossRefGoogle Scholar
  12. Benitez S, Lagos N A, Osores S, Opitz T, Duarte C, Navarro J M, Lardies M A. 2018. High/pCO2 levels affect metabolic rate, but not feeding behavior and fitness, of farmed giant mussel Choromytilus chorus. Aquae. Environ. Interact., 10: 267–278,  https://doi.org/10.3354/aei00271.CrossRefGoogle Scholar
  13. Bergan A J, Lawson G L, Maas A E, Wang Z A. 2017. The effect of elevated carbon dioxide on the sinking and swimming of the shelled pteropod Limacina retroversa. ICES J. Mar. Sci., 74(7): 1893–1905,  https://doi.org/10.1093/icesjms/fsx008.CrossRefGoogle Scholar
  14. Bibby R, Cleall-Harding P, Rundle S, Widdicombe S, Spicer J. 2007. Ocean acidification disrupts induced defences in the intertidal gastropod Littorina littorea. Biol. Lett., 3(6): 699–701,  https://doi.org/10.1098/rsbl.2007.0457.CrossRefGoogle Scholar
  15. Boron W F. 1987. Intracellular pH regulation. In: Andreoli T E, Hoffman J F, Fanestil D D, Schultz S G eds. Membrane Transport Processes in Organized Systems. Springer, Boston, MA. p.39–51,  https://doi.org/10.1007/978-l-4684-5404-8_3.CrossRefGoogle Scholar
  16. Brennand H S, Soars N, Dworjanyn S A, Davis A R, Byrne M. 2010. Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. PLoS One, 5(6): e. 1372.  https://doi.org/10.1371/journal.pone.0011372.
  17. Briffa M, De La Haye K, Munday P L. 2012. High CO2 and marine animal behaviour: potential mechanisms and ecological consequences. Mar. Pollut. Bull, 64(8): 1519–1528,  https://doi.org/10.1016/j.marpolbul.2012.05.032.CrossRefGoogle Scholar
  18. Burnell O W, Russell B D, Irving A D, Cornell S D. 2013. Eutrophication offsets increased sea urchin grazing on seagrass caused by ocean warming and acidification. Mar. Ecol. Prog. Ser., 485: 37–46,  https://doi.org/10.3354/mepsl0323.CrossRefGoogle Scholar
  19. Caley M J, Carr M H, Hixon M A, Hughes T P, Jones G R Menge B A. 1996. Recruitment and the local dynamics of open marine populations. Annu. Rev. Ecol. Syst., 27: 477–500,  https://doi.org/10.1146/annurev.ecolsys.27.1.477.CrossRefGoogle Scholar
  20. Carroll M A, Catapane E J, Molecular. 2007. The nervous system control of lateral ciliary activity of the gill of the bivalve mollusc, Crassostrea virginica. Comp. Biochem. Physiol. A: Mol. Integr. Physiol., 148(2): 445–450,  https://doi.org/10.1016/j.cbpa.2007.06.003.CrossRefGoogle Scholar
  21. Catapane E J, Nelson M, Adams T, Carroll M A. 2016. Innervation of gill lateral cells in the bivalve mollusc Crassostrea virginica affects cellular membrane potential and cilia activity. J. Pharmacol. Rep., 1(2): 109.Google Scholar
  22. Catapane E J, Stefano G B, Aiello E. 1978. Pharmacological study of the reciprocal dual innervation of the lateral ciliated gill epithelium by the CNS of Mytilus edulis (Bivalvia). J. Exp. Biol, 74(1): 101–113.Google Scholar
  23. Catapane E J, Stefano G B, Aiello E. 1979. Neurophysiological correlates of the dopaminergic cilio-inhibitory mechanism of Mytilus edulis. J. Exp. Biol., 83: 315–323.Google Scholar
  24. Chan K Y K, García E, Dupont S. 2015. Acidification reduced growth rate but not swimming speed of larval sea urchins. Sci. Rep., 5: 9764,  https://doi.org/10.1038/srep09764.CrossRefGoogle Scholar
  25. Chan K Y K, Grünbaum D, Arnberg M, Dupont S. 2016. Impacts of ocean acidification on survival, growth, and swimming behaviours differ between larval urchins and brittlestars. ICES J. Mar. Sci., 73(3): 951–961,  https://doi.org/10.1093/icesjms/fsv073.CrossRefGoogle Scholar
  26. Chan K Y K, Grunbaum D, O’Donnell M J. 2011. Effects of ocean-acidification-induced morphological changes on larval swimming and feeding. J. Exp. Biol., 214(22): 3857–3867,  https://doi.org/10.1242/jeb.054809.CrossRefGoogle Scholar
  27. Charpentier C L, Cohen J H. 2016. Acidification and y-aminobutyric acid independently alter kairomone-induced behaviour. R. Soc. Open Sci., 3(9): 160–311,  https://doi.org/10.1098/rsos.l60311.CrossRefGoogle Scholar
  28. Chivers D P, McCormick M I, Nilsson G E, Munday P L, Watson S A, Meekan M G, Mitchell M D, Corkill K C, Ferrari M C O. 2014. Impaired learning of predators and lower prey survival under elevated CO2: a consequence of neurotransmitter interference. Global Change Biol, 20(2): 515–522,  https://doi.org/10.1111/gcb.12291.CrossRefGoogle Scholar
  29. Christmas A M F. 2013. Effects of Ocean Acidification on Dispersal Behavior in the Larval Stage of the Dungeness Crab and the Pacific Green Shore Crab. Western Washington University, Bellingham.Google Scholar
  30. Chung W S, Marshall N J, Watson S A, Munday P L, Nilsson G E. 2014. Ocean acidification slows retinal function in a damselfish through interference with GABAA receptors. J. Exp. Biol, 217(3): 323–326,  https://doi.org/10.1242/jeb.092478.CrossRefGoogle Scholar
  31. Cigliano M, Gambi M C, Rodolfo-Metalpa R, Patti F R Hall-Spencer J M. 2010. Effects of ocean acidification on invertebrate settlement at volcanic C02 vents. Mar. Biol, 157(11): 2489–2502,  https://doi.org/10.1007/s00227-010-1513-6.CrossRefGoogle Scholar
  32. Clements J C, Bishop M M, Hunt H L. 2017. Elevated temperature has adverse effects on GABA-mediated avoidance behaviour to sediment acidification in a wide-ranging marine bivalve. Mar. Biol, 164(3): 56,  https://doi.org/10.1007/s00227-017-3085-1.CrossRefGoogle Scholar
  33. Clements J C, Hunt H L. 2014. Influence of sediment acidification and water flow on sediment acceptance and dispersal of juvenile soft-shell clams (Mya arenaria L.). J. Exp. Mar. Biol. Ecol, 453: 62–69,  https://doi.org/10.1016/j.jembe.2014.01.002.CrossRefGoogle Scholar
  34. Clements J C, Hunt H L. 2015. Marine animal behaviour in a high CO2 ocean. Mar. Ecol. Prog. Ser., 536: 259–279,  https://doi.org/10.3354/mepsll426.CrossRefGoogle Scholar
  35. Clements J C, Hunt H L. 2017. Effects of CO2-driven sediment acidification on infaunal marine bivalves: a synthesis. Mar. Pollut. Bull., 117(1-2): 6–16,  https://doi.org/10.1016/j.marpolbul.2017.01.053.CrossRefGoogle Scholar
  36. De La Haye K L, Spicer J I, Widdicombe S, Briffa M. 2011. Reduced sea water pH disrupts resource assessment and decision making in the hermit crab Pagurus bernhardus. Anim. Behav., 82(3): 495–501,  https://doi.org/10.1016/.anbehav.2011.05.030.CrossRefGoogle Scholar
  37. De La Haye K L, Spicer J I, Widdicombe S, Briffa M. 2012. Reduced pH sea water disrupts chemo-responsive behaviour in an intertidal crustacean. J. Exp. Mar. Biol Ecol., 412: 134–140,  https://doi.org/10.1016/j.jembe.2011.11.013.CrossRefGoogle Scholar
  38. Devine B M, Munday P L, Jones G P. 2012. Rising CO2 concentrations affect settlement behaviour of larval damselfishes. Coral Reefs, 31(1): 229–238,  https://doi.org/10.1007/s00338-011-0837-0.CrossRefGoogle Scholar
  39. Dissanayake A, Ishimatsu A. 2011. Synergistic effects of elevated CO2 and temperature on the metabolic scope and activity in a shallow-water coastal decapod (Metapenaeus joyneri; Crustacea: Penaeidae). ICES J. Mar. Sci., 68(6): 1147–1154,  https://doi.org/10.1093/icesjms/fsql88.CrossRefGoogle Scholar
  40. Domenici P, Torres R, Manriquez P H. 2017. Effects of elevated carbon dioxide and temperature on locomotion and the repeatability of lateralization in a keystone marine mollusc. J. Exp. Biol, 220(4): 667–676,  https://doi.org/10.1242/jeb.l51779.CrossRefGoogle Scholar
  41. Doropoulos C, Diaz-Pulido G. 2013. High CO2 reduces the settlement of a spawning coral on three common species of crustose coralline algae. Mar. Ecol. Prog. Ser, 475: 93–99,  https://doi.org/10.3354/mepsl0096.CrossRefGoogle Scholar
  42. Doropoulos C, Ward S, Diaz-Pulido G, Hoegh-Guldberg O, Mumby P J. 2012. Ocean acidification reduces coral recruitment by disrupting intimate larval-algal settlement interactions. Ecol. Lett., 15(4): 338–346,  https://doi.org/10.1111/j.l461-0248.2012.01743.x.CrossRefGoogle Scholar
  43. Duarte C, Lopez J, Benitez S, Manriquez P H, Navarro J M, Bonta C C, Torres R, Quijon P. 2016. Ocean acidification induces changes in algal palatability and herbivore feeding behavior and performance. Oecologia, 180(2): 453–462,  https://doi.org/10.1007/s00442-015-3459-3.CrossRefGoogle Scholar
  44. Dupont S T, Mercurio M, Giacoletti A, Rinaldi A, Mirto S, D’Acquisto L, Sabatino MA, Sara G. 2015. Functional consequences of prey acclimation to ocean acidification for the prey and its predator. PeerJ PrePr., 3: el438vl.Google Scholar
  45. Dupont S, Havenhand J, Thorndyke W, Peck L S, Thorndyke M. 2008. Near-future level of CO2-driven ocean acidification radically affects larval survival and development in the brittlestar Ophiothrix fragilis. Mar. Ecol. Prog. Ser, 373: 285–294.CrossRefGoogle Scholar
  46. Eads A R, Kennington W J, Evans J P. 2016. Interactive effects of ocean warming and acidification on sperm motility and fertilization in the mussel Mytilus galloprovincialis. Mar. Ecol. Prog. Ser., 562: 101–111,  https://doi.org/10.3354/mepsll944.CrossRefGoogle Scholar
  47. Elgeti J, Winkler R G, Gompper G. 2015. Physics of microswimmers—single particle motion and collective behavior: a review. Rep. Prog. Phys., 78(5). 056601.  https://doi.org/10.1088/0034-4885/78/5/056601.
  48. Ellis R P, Bersey J, Rundle S D, Hall-Spencer J M, Spicer J I. 2009. Subtle but significant effects of CO2 acidified seawater on embryos of the intertidal snail, Littorina obtusata. Aquat. Biol., 5(1): 41–48,  https://doi.org/10.3354/ab00118.CrossRefGoogle Scholar
  49. Fabry V J, Seibel B A, Feely R A, Orr J C. 2008. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J. Mar. Sci., 65(3): 414–432,  https://doi.org/10.1093/icesjms/fsn048.CrossRefGoogle Scholar
  50. Ferrari M C O, McCormick M I, Munday P L, Meekan M G, Dixson D L, Lonnstedt O, Chivers D P. 2012. Effects of ocean acidification on visual risk assessment in coral reef fishes. FunctEcol, 26(3): 553–558,  https://doi.org/10.1111/J.1365-2435.2011.01951.X.CrossRefGoogle Scholar
  51. Garcia E, Clemente S, Carlos Hernández J. 2018. Effects of natural current pH variability on the sea urchin Paracentrotus lividus larvae development and settlement. Mar. Environ. Res., 139: 11–18,  https://doi.org/10.1016/j.marenvres.2018.04.012.CrossRefGoogle Scholar
  52. Glaspie C N, Longmire K, Seitz R D. 2017. Acidification alters predator-prey interactions of blue crab Callinectes sapidus and soft-shell clam Mya arenaria. J. Exp. Mar. Biol. Ecol, 489: 58–65,  https://doi.org/10.1016/jjembe.2016.11.010.CrossRefGoogle Scholar
  53. Gonzalez-Gurriarán E, Freire J, Bernardez C. 2002. Migratory patterns of female spider crabs Maja squinado detected using electronic tags and telemetry. J. Crustacean Biol, 22(1): 91–97,  https://doi.org/10.1163/20021975-99990212.CrossRefGoogle Scholar
  54. Gosselin L A, Qian P Y. 1997. Juvenile mortality in benthic marine invertebrates. Mar. Ecol. Prog. Ser., 146: 265–282,  https://doi.org/10.3354/mepsl46265.CrossRefGoogle Scholar
  55. Gray M W, Langdon C J, Waldbusser G G, Hales B, Kramer S. 2017. Mechanistic understanding of ocean acidification impacts on larval feeding physiology and energy budgets of the mussel Mytilus californianus. Mar. Ecol. Prog. Ser, 563: 81–94,  https://doi.org/10.3354/mepsll977.CrossRefGoogle Scholar
  56. Green M A, Waldbusser G G, Hubazc L, Cathcart E, Hall J. 2013. Carbonate mineral saturation state as the recruitment cue for settling bivalves in marine muds. Estuar. Coasts, 36(1): 18–27,  https://doi.org/10.1007/sl2237-012-9549-0.CrossRefGoogle Scholar
  57. Green M A, Waldbusser G G, Reilly S L, Emerson K, O’Donnell S. 2009. Death by dissolution: sediment saturation state as a mortality factor for juvenile bivalves. Limnol. Oceanogr., 54(4): 1037–1047,  https://doi.org/10.4319/10.2009.54.4.1037.CrossRefGoogle Scholar
  58. Hamilton T J, Holcombe A, Tresguerres M. 2013. CO2-induced ocean acidification increases anxiety in rockfish via alteration of GABAA receptor functioning. Proc. Biol. Sci., 281(1775). 20132509.  https://doi.org/10.1098/rspb.2013.2509.
  59. Havenhand J N, Buttler F R, Thorndyke M C, Williamson J E. 2008. Near-future levels of ocean acidification reduce fertilization success in a sea urchin. Curr. Biol, 18(15): R651–R652,  https://doi.org/10.1016/j.cub.2008.06.015.CrossRefGoogle Scholar
  60. Havenhand J N, Schlegel P. 2009. Near-future levels of ocean acidification do not affect sperm motility and fertilization kinetics in the oyster Crassostrea gigas. Biogeosciences, 6(12): 3009–3015,  https://doi.org/10.5194/bg-6-3009-2009.CrossRefGoogle Scholar
  61. Heuer R M, Grosell M. 2014. Physiological impacts of elevated carbon dioxide and ocean acidification on fish. Am. J. Physiol. - Regul Integr. Comp. Physiol, 307(9): R1 061–R1 084,  https://doi.org/10.1152/ajpregu.00064.2014.CrossRefGoogle Scholar
  62. Huijbers C M, Nagelkerken I, Lössbroek P A C, Schulten I E, Siegenthaler A, Holderied M W, Simpson S D. 2012. A test of the senses: fish select novel habitats by responding to multiple cues. Ecology, 93(1): 46–55.CrossRefGoogle Scholar
  63. Hunt H L, Scheibling R E. 1997. Role of early post-settlement mortality in recruitment of benthic marine invertebrates. Mar. Ecol. Prog. Ser, 155: 269–301,  https://doi.org/10.3354/mepsl55269.CrossRefGoogle Scholar
  64. Igulu M M, Nagelkerken, I, Beek, M V D, Schippers, M, Eck, R.V, Mgaya, Y D. 2013. Orientation from open water to settlement habitats by coral reef fish: behavioral flexibility in the use of multiple reliable cues. Mar. Ecol. Prog. Ser., 493: 243–257,  https://doi.org/10.3354/mepsl0542.CrossRefGoogle Scholar
  65. Igulu, M M, Nagelkerken, I, Fraaije, R, Hintum, R V, Ligtenberg, H, Mgaya, YD. 2011. The potential role of visual cues for microhabitat selection during the early life phase of a coral reef fish (Lutjanus fulviflamma). J. Exp. Mar. Biol. Ecol, 401: 118–125,  https://doi.org/10.1016/).jembe.2011.01.022.CrossRefGoogle Scholar
  66. Jellison B M, Ninokawa A T, Hill T M, Sanford E, Gay lord B. 2016. Ocean acidification alters the response of intertidal snails to a key sea star predator. Proc. Biol. Sci., 283(1833). 20160890.  https://doi.org/10.1098/rspb.2016.0890.
  67. lessen K R, Mirsky R, Dennison M E, Burnstock G. 1979. GABA may be a neurotransmitter in the vertebrate peripheral nervous system. Nature, 281(5726): 71–74,  https://doi.org/10.1038/281071a0.CrossRefGoogle Scholar
  68. Kim T W, Barry J P. 2016. Boldness in a deep sea hermit crab to simulated tactile predator attacks is unaffected by ocean acidification. Ocean Sci. J., 51(3): 381–386,  https://doi.org/10.1007/sl2601-016-0034-8.CrossRefGoogle Scholar
  69. Kroeker K J, Kordas R L, Crim R N, Singh G G. 2010. Metaanalysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol. Lett., 13(11): 1419–1434,  https://doi.org/10.1111/j.1461-0248.2010.01518.x.CrossRefGoogle Scholar
  70. Kroeker K J, Kordas R L, Crim R, Hendriks I E, Ramajo L, Singh G S, Duarte C M, Gattuso J P. 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Global Change Biol., 19(6): 1884–1896,  https://doi.org/10.1111/gcb.12179.CrossRefGoogle Scholar
  71. Kroeker K J, Sanford E, Jellison B M, Gaylord B. 2014. Predicting the effects of ocean acidification on predator-prey interactions: a conceptual framework based on coastal molluscs. Biol. Bull., 226(3): 211–222,  https://doi.org/10.1086/BBLv226n3p211.CrossRefGoogle Scholar
  72. Lai F, Jutfelt F, Nilsson G E. 2015. Altered neurotransmitter function in CO2-exposed stickleback (Gasterosteus aculeatus): a temperate model species for ocean acidification research. Conserv. Physiol., 3(1): cov018,  https://doi.org/10.1093/conphys/cov018.
  73. Landes A, Zimmer M. 2012. Acidification and warming affect both a calcifying predator and prey, but not their interaction. Mar. Ecol. Prog. Ser, 450: 1–10,  https://doi.org/10.3354/meps09666.CrossRefGoogle Scholar
  74. Li L S, Lu W Q, Sui Y M, Wang Y J, Gul Y, Dupont S. 2015. Conflicting effects of predator cue and ocean acidification on the mussel Mytilus coruscus byssus production. J. ShellfishRes., 34(2): 393–400,  https://doi.org/10.2983/035.034.0222.CrossRefGoogle Scholar
  75. Li W, Gao K. 2012. A marine secondary producer respires and feeds more in a high CO2 ocean. Mar. Pollut. Bull., 64(4): 699–703,  https://doi.org/10.1016/j.marpolbul.2012.01.033.CrossRefGoogle Scholar
  76. Lohmann K J, Lohmann C M F, Endres C S. 2008. The sensory ecology of ocean navigation. J. Exp. Biol., 211(11): 1719–1728,  https://doi.org/10.1242/jeb.015792.CrossRefGoogle Scholar
  77. Lunt G G. 1991. GABA and GABA receptors in invertebrates. Semin. Neurosci., 3(3): 251–258,  https://doi.org/10.1016/1044-5765(91)90022-G.CrossRefGoogle Scholar
  78. Maboloc E A, Chan K Y K. 2017. Resilience of the larval slipper limpet Crepidula onyx to direct and indirect-diet effects of ocean acidification. Sci. Rep., 7(1): 12062,  https://doi.org/10.1038/s41598-017-12253-2.
  79. Manriquez P H, Jara M E, Mardones M L, Navarro J M, Torres R, Lardies M A, Vargas C A, Duarte C, Widdicombe S, Salisbury J, Lagos N A. 2013. Ocean acidification disrupts prey responses to predator cues but not net prey shell growth in Concholepas concholepas (loco). PLoS One, 8(7): e68643.Google Scholar
  80. Manriquez P H, Jara M E, Mardones M L, Torres R, Navarro J M, Lardies M A, Vargas C A, Duarte C, Lagos N A. 2014. Ocean acidification affects predator avoidance behaviour but not prey detection in the early ontogeny of a keystone species. Mar. Ecol. Prog. Ser., 502: 157–167,  https://doi.org/10.3354/mepsl0703.CrossRefGoogle Scholar
  81. Manriquez P H, Jara M E, Seguel M E, Torres R, Alarcon E, Lee M R. 2016. Ocean acidification and increased temperature have both positive and negative effects on early ontogenetic traits of a rocky shore keystone predator species. PLoS One, 11(3): e0151920,  https://doi.org/10.1371/journal.pone.0151920.
  82. Morse B, Rochette R. 2016. Movements and activity levels of juvenile American lobsters Homarus americanus in nature quantified using ultrasonic telemetry. Mar. Ecol. Prog. Ser, 551: 155–170,  https://doi.org/10.3354/mepsll721.CrossRefGoogle Scholar
  83. Nagelkerken I, Munday P L. 2016. Animal Behaviour shapes the ecological effects of ocean acidification and warming: moving from individual to community-level responses. Global Change Biol, 22(3): 974–989,  https://doi.org/10.1111/gcb.l3167.CrossRefGoogle Scholar
  84. Nakamura M, Ohki S, Suzuki A, Sakai K. 2011. Coral larvae under ocean acidification: survival, metabolism, and metamorphosis. PLoS One, 6(1): el4521,  https://doi.org/10.1371/journal.pone.0014521.
  85. Nilsson G E, Dixson D L, Domenici P, McCormick M I, Serensen C, Watson S A, Munday P L. 2012. Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nat. Clim. Change, 2(3): 201–204,  https://doi.org/10.1038/nclimatel352.CrossRefGoogle Scholar
  86. Ohman M D, Frost B W, Cohen E B. 1983. Reverse diel vertical migration: an escape from invertebrate predators. Science, 220(4604): 1404–1407,  https://doi.org/10.1126/science.220.4604.1404.CrossRefGoogle Scholar
  87. Ou M, Hamilton T J, Eom J, Lyall E M, Gallup J, Jiang A, Lee J, Close DA, Yun S S, Brauner C J. 2015. Responses of pink salmon to CO2-induced aquatic acidification. Nat. Clim. Change, 5(10): 950–955,  https://doi.org/10.1038/nclimate2694.CrossRefGoogle Scholar
  88. Pecquet A, Dorey N, Chan K Y K. 2017. Ocean acidification increases larval swimming speed and has limited effects on spawning and settlement of a robust fouling bryozoan, Bugula neritina. Mar. Pollut. Bull., 124(2): 903–910,  https://doi.org/10.1016/j.marpolbul.2017.02.057.CrossRefGoogle Scholar
  89. Peng C, Zhao X G, Liu S X, Shi W, Han Y, Guo C, Peng X, Chai X L, Liu G X. 2017. Ocean acidification alters the burrowing behaviour, Ca2+/Mg2+-ATPase activity, metabolism, and gene expression of a bivalve species, Sinonovacula constricta. Mar. Ecol. Prog. Ser., 575: 107–117,  https://doi.org/10.3354/mepsl2224.CrossRefGoogle Scholar
  90. Persons M H, Walker S E, Rypstra A L, Marshall S D. 2001. Wolf spider predator avoidance tactics and survival in the presence of diet-associated predator cues (Araneae: Lycosidae). Anim. Behav., 61(1): 43–51,  https://doi.org/10.1006/anbe.2000.1594.CrossRefGoogle Scholar
  91. Pilditch C A, Valanko S, Norkko J, Norkko A. 2015. Post-settlement dispersal: the neglected link in maintenance of soft-sediment biodiversity. Biol. Lett., 11(2). 20140795.  https://doi.org/10.1098/rsbl.2014.0795.
  92. Queiros A M, Fernandes J A, Faulwetter S, Nunes J, Rastrick S P S, Meszkowska N, Artioli Y, Yool A, Calosi P, Arvanitidis C, Findlay H S, Barange M, Cheung W W L, Widdicombe S. 2015. Scaling up experimental ocean acidification and warming research: from individuals to the ecosystem. Global Change Biol., 21(1): 130–143,  https://doi.org/10.1111/gcb.12675.CrossRefGoogle Scholar
  93. Quinn B K, Rochette R. 2015. Potential effect of variation in water temperature on development time of American lobster larvae. ICES J. Mar. Sci., 72(S1): i79–i90,  https://doi.org/10.1093/icesjms/fsv010.CrossRefGoogle Scholar
  94. Quinn B. 2014. Assessing Potential Influence of Larval Development Time and Drift on Large-scale Spatial Connectivity of American Lobster (Homarus americanus). University of New Brunswick, Fredericton and Saint John, NB.Google Scholar
  95. Ren Z, Mu C, Li R, Song W, Wang C. 2018. Characterization of a γ-aminobutyrate type A receptor-associated protein gene, which is involved in the response of Portunus trituberculatus to CO2-induced ocean acidification. Aquat. Res., 49(7): 2393–2403,  https://doi.org/10.1111/are.13699.CrossRefGoogle Scholar
  96. Rodriguez S R, Ojeda F P, InestrosaN C. 1993. Settlement of benthic marine invertebrates. Mar. Ecol. Prog. Ser., 97: 193–207,  https://doi.org/10.3354/meps097193.CrossRefGoogle Scholar
  97. Roggatz C C, Lorch M, Hardege J D, Benoit D M. 2016. Ocean acidification affects marine chemical communication by changing structure and function of peptide signalling molecules. Global Change Biol., 22(12): 3914–3926,  https://doi.org/10.1111/gcb.13354.CrossRefGoogle Scholar
  98. Saba G K, Schofield O, Torres J J, Ombres E H, Steinberg D K. 2012. Increased feeding and nutrient excretion of adult Antarctic krill, Euphausia superba, exposed to enhanced carbon dioxide (CO2). PLoS One, 7(12): e52224,  https://doi.org/10.1371/journal.pone.0052224.
  99. Sanford E, Gaylord B, Hettinger A, Lenz E A, Meyer K, Hill T M. 2014. Ocean acidification increases the vulnerability of native oysters to predation by invasive snails. Proc. Biol. Sci., 281(1778). 20132681.  https://doi.org/10.1098/rspb.2013.2681.
  100. Schalkhausser B, Bock C, Stemmer K, Brey T, Portner H O, Lannig G B. 2013. Impact of ocean acidification on escape performance of the king scallop, Pecten maximus, from Norway. Mar. Biol, 160(8): 1995–2006,  https://doi.org/10.1007/s00227-012-2057-8.CrossRefGoogle Scholar
  101. Schlegel P, Binet M T, Havenhand J N, Doyle C J, Williamson J E. 2015. Ocean acidification impacts on sperm mitochondrial membrane potential bring sperm swimming behaviour near its tipping point. J. Exp. Biol., 218(7): 1084–1090,  https://doi.org/10.1242/jeb.114900.CrossRefGoogle Scholar
  102. Schram J B, Schoenrock K M, McClintock J B, Amsler C D, Angus R A. 2017. Ocean warming and acidification alter Antarctic macroalgal biochemical composition but not amphipod grazer feeding preferences. Mar. Ecol. Prog. Ser., 581: 45–56,  https://doi.org/10.3354/mepsl2308.CrossRefGoogle Scholar
  103. Shi W, Han Y, Guo C, Zhao X G, Liu S X, Su W H, Wang Y C, Zha S J, Chai X L, Liu G X. 2017a. Ocean acidification hampers sperm-egg collisions, gamete fusion, and generation of Ca2+ oscillations of a broadcast spawning bivalve, Tegillarca granosa. Mar. Environ. Res., 130: 106–112,  https://doi.org/10.1016/j.marenvres.2017.07.016.CrossRefGoogle Scholar
  104. Shi W, Zhao X G, Han Y, Guo C, Liu S X, Su S H, Wang Y C, Zha S J, Chai X L, Fu W D, Yang H C, Liu G X. 2017b. Effects of reduced pH and elevated pCO2 on sperm motility and fertilisation success in blood clam, Tegillarca granosa. N. Z. J. Mar. Freshwater Res., 51(4): 543–554,  https://doi.org/10.1080/00288330.2017.1296006.CrossRefGoogle Scholar
  105. Sih A, Bell A, Johnson J C. 2004. Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol. Evol., 19(7): 372–378,  https://doi.org/10.1016/j.tree.2004.04.009.CrossRefGoogle Scholar
  106. Smee D L, Weissburg M J. 2006. Hard clams (Mercenaria mercenaria) evaluate predation risk using chemical signals from predators and injured conspecifics. J. Chem. Ecol, 32(3): 605–619,  https://doi.org/10.1007/sl0886-005-9021-8.CrossRefGoogle Scholar
  107. Spady B L, Munday P L, Watson S A. 2018. Predatory strategies and behaviours in cephalopods are altered by elevated CO2. Global Change Biol, 24(6): 2585–2596,  https://doi.org/10.1111/gcb.14098.CrossRefGoogle Scholar
  108. Spady B L, Watson S A, Chase T J, Munday P L. 2014. Projected near-future CO2 levels increase activity and alter defensive behaviours in the tropical squid Idiosepius pygmaeus. Biol. Open, 3(11): 1063–1070,  https://doi.org/10.1242/bio.20149894.CrossRefGoogle Scholar
  109. Sui Y M, Hu M H, Huang X Z, Wang Y J, Lu W Q. 2015. Anti-predatory responses of the thick shell mussel Mytilus coruscus exposed to seawater acidification and hypoxia. Mar. Environ. Res., 109: 159–167,  https://doi.org/10.1016/j.marenvres.2015.07.008.CrossRefGoogle Scholar
  110. Sui Y M, Liu Y M, Zhao X, Dupont S, Hu M H, Wu F L, Huang X Z, Li J L, Lu W Q, Wang Y J. 2017. Defense responses to short-term hypoxia and seawater acidification in the thick shell mussel Mytilus coruscus. Front. Physiol, 8: 145,  https://doi.org/10.3389/fphys.2017.00145.Google Scholar
  111. Sunday J M, Fabricius K E, Kroeker K J, Anderson K M, Brown N E, Barry J P, Connell S D, Dupont S, Gaylord B, Hall-Spencer J M, Klinger T, Milazzo M, Munday P L, Russell B D, Sanford E, Thiyagarajan V, Vaughan M L H, Widdicombe S, Harley C D G. 2017. Ocean acidification can mediate biodiversity shifts by changing biogenic habitat. Nat. Clim. Change, 7(1): 81–85,  https://doi.org/10.1038/NCLIMATE3161.CrossRefGoogle Scholar
  112. Talmage S C, Gobler C J. 2010. Effects of past, present, and future ocean carbon dioxide concentrations on the growth and survival of larval shellfish. Proc. Natl. Acad. Sci. USA, 107(40): 17246–17251,  https://doi.org/10.1073/pnas.0913804107.CrossRefGoogle Scholar
  113. Tierney A J, Atema T. 1988. Amino acid chemoreception: effects of pH on receptors and stimuli. J. Chem. Ecol, 14(1): 135–141,  https://doi.org/10.1007/BF01022537.CrossRefGoogle Scholar
  114. Uthicke S, Pecorino D, Albright R, Negri A P, Cantin N, Liddy M, Dworjanyn S, Kamya P, Byrne M, Lamare M. 2013. Impacts of ocean acidification on early life-history stages and settlement of the coral-eating sea star Acanthaster planci. PLoS One, 8(12): e82938,  https://doi.org/10.1371/journal.pone.0082938.
  115. Vargas C A, Aguilera V M, Martin V S, Manriquez P H, Navarro J M, Duarte C, Torres R, Lardies MA, Lagos N A. 2015. CO2-driven ocean acidification disrupts the filter feeding behavior in Chilean gastropod and bivalve species from different geographic localities. Estuar. Coasts, 38(4): 1163–1177.CrossRefGoogle Scholar
  116. Vargas C A, De La Hoz M, Aguilera V, Martin V S, Manriquez P H, Navarro J M, Torres R, Lardies M A, Lagos N A. 2013. CO2-driven ocean acidification reduces larval feeding efficiency and changes food selectivity in the mollusk Concholepas concholepas. J. Plankton Res., 35(5): 1059–1068,  https://doi.org/10.1093/plankt/fbt045.CrossRefGoogle Scholar
  117. Vargas C A, Lagos N A, Lardies M A, Duarte C, Manriquez P H, Aguilera V M, Broitman B, Widdicombe S, Dupont S. 2017. Species-specific responses to ocean acidification should account for local adaptation and adaptive plasticity. Nat.Ecol.Evol., 1(4): 84,  https://doi.org/10.1038/s41559-017-0084.CrossRefGoogle Scholar
  118. Viyakarn V, Lalitpattarakit W, Chinfak N, Jandang S, Kuanui P, Khokiattiwong S, Chavanich S. 2015. Effect of lower pH on settlement and development of coral, Pocillopora damicornis (Linnaeus, 1758). Ocean Sci. J.50(2): 475–480.CrossRefGoogle Scholar
  119. Wang Y J, Hu M H, Wu F L, Starch D, Portner H O. 2018. Elevated pCO 2 affects feeding behavior and acute physiological response of the brown crab Cancer pagurus. Front. Physiol, 9: 1164.CrossRefGoogle Scholar
  120. Wang Y J, Li L S, Hu M H, Lu W Q. 2015. Physiological energetics of the thick shell mussel Mytilus coruscus exposed to seawater acidification and thermal stress. Sci. Total Environ., 514: 261–272,  https://doi.org/10.1016/scitotenv.2015.01.092.CrossRefGoogle Scholar
  121. Watson S A, Fields J B, Munday P L. 2017. Ocean acidification alters predator behaviour and reduces predation rate. Biol. Lett., 13(2). 20160797.  https://doi.org/10.1098/rsbl.2016.0797.
  122. Watson S A, Lefevre S, McCormick M I, Domenici P, Nilsson G E, Munday P L. 2014. Marine mollusc predator-escape behaviour altered by near-future carbon dioxide levels. Proc. Biol. Sci., 281(1774). 20132377.  https://doi.org/10.1098/rspb.2013.2377.
  123. Webster N S, Uthicke S, Botte E S, Flores F, Negri A P. 2013. Ocean acidification reduces induction of coral settlement by crustose coralline algae. Global Change Biol., 19(1): 303–315,  https://doi.org/10.1111/gcb.12008.CrossRefGoogle Scholar
  124. Widdicombe S, Needham H R. 2007. Impact of CO2-induced seawater acidification on the burrowing activity of Nereis virens and sediment nutrient flux. Mar. Ecol. Prog. Ser., 341: 111–122,  https://doi.org/10.3354/meps341111.CrossRefGoogle Scholar
  125. Widdicombe S, Spicer J I. 2008. Predicting the impact of ocean acidification on benthic biodiversity: what can animal physiology tell us? J. Exp. Mar. Biol. Ecol, 366(1-2): 187–197,  https://doi.org/10.1016/j.jembe.2008.07.024.CrossRefGoogle Scholar
  126. Wright J M, O’Connor W A, Parker L M, Ross P M. 2018a. Predation by the endemic whelk Tenguella marginalba (Blainville. 1832). on the invasive Pacific oyster Crassostrea gigas (Thunberg, 1793). Molluscan Res., 38(2): 130–136,  https://doi.org/10.1080/13235818.2017.1420397.CrossRefGoogle Scholar
  127. Wright J M, Parker L M, O’Connor W A, Scanes E, Ross P M. 2018b. Ocean acidification affects both the predator and prey to alter interactions between the oyster Crassostrea gigas (Thunberg. 1793). and the whelk Tenguella marginalba (Blainville, 1832). Mar. Biol, 165(3): 46,  https://doi.org/10.1007/s00227-018-3302-6.Google Scholar
  128. Wu F L, Wang T, Cui S K, Xie Z, Dupont S, Zeng J N, Gu H X, Kong H, Hu M H, Lu W Q, Wang Y J. 2017. Effects of seawater pH and temperature on foraging behavior of the Japanese stone crab Charybdis japonica. Mar. Pollut. Bull, 120(1-2): 99–108,  https://doi.org/10.1016/j.marpolbul.2017.04.053.CrossRefGoogle Scholar
  129. Xu X Y, Yip K R, Shin P K S, Cheung S G. 2017. Predator-prey interaction between muricid gastropods and mussels under ocean acidification. Mar. Pollut. Bull, 124(2): 911–916,  https://doi.org/10.1016/j.marpolbul.2017.01.003.CrossRefGoogle Scholar
  130. Xu X, Yang F, Zhao L Q, Yan X W. 2016. Seawater acidification affects the physiological energetics and spawning capacity of the Manila clam Ruditapes philippinarum during gonadal maturation. Comp. Biochem. Physiol. A: Mol Integr. Physiol, 196: 20–29,  https://doi.org/10.1016/j.cbpa.2016.02.014.CrossRefGoogle Scholar
  131. Zhao X G, Guo C, Han Y, Che Z M, Wang Y C, Wang X Y, Chai X L, Wu H X, Liu G X. 2017b. Ocean acidification decreases mussel byssal attachment strength and induces molecular byssal responses. Mar. Ecol. Prog. Ser., 565: 67–77,  https://doi.org/10.3354/mepsl1992.CrossRefGoogle Scholar
  132. Zhao X G, Shi W, Han Y, Liu S X, Guo C, Fu W D, Chai X L, Liu G X. 2017a. Ocean acidification adversely influences metabolism, extracellular pH and calcification of an economically important marine bivalve, Tegillarca granosa. Mar. Environ. Res., 125: 82–89,  https://doi.org/10.1016/j.marenvres.2017.01.007.CrossRefGoogle Scholar
  133. Zittier Z M C, Hirse T, Portner H. 2013. The synergistic effects of increasing temperature and CO2 levels on activity capacity and acid-base balance in the spider crab, Eyas araneus. Mar. Biol, 160(8): 2049–2062,  https://doi.org/10.1007/s00227-012-2073-8.CrossRefGoogle Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.National Demonstration Center for Experimental Fisheries Science Education (Shanghai Ocean University)ShanghaiChina
  2. 2.International Research Center for Marine Biosciences at Shanghai Ocean University, Ministry of Science and TechnologyShanghaiChina
  3. 3.Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources (Shanghai Ocean University), Ministry of EducationShanghaiChina

Personalised recommendations